Dynamic interpretation of maternal inputs by the Drosophila segmentation gene network

Feng Liu, Alexander H. Morrison and Thomas Gregor, PNAS 110: 6724–6729 (2013).

Patterning in multicellular organisms relies on the interpretation of transcription factor (TF) concentrations by genetic networks. To determine the extent by which absolute TF concentration dictates gene expression and morphogenesis programs in Drosophila embryos, we manipulate maternally supplied patterning determinants and measure readout concentration at the position of various patterning markers. When we increase the overall amount of the maternal TF bicoid 5-fold, Bicoid concentrations in cells at positions of the cephalic furrow, an early morphological marker, differ by a factor of two, apparently contradicting the traditional threshold-dependent readout model. In contrast, Bicoid concentration at target gene expression boundaries is nearly unchanged during early developmental times, but adjusts dynamically toward the same 2-fold change as development progresses. Thus the Drosophila segmentation gene network responds faithfully to Bicoid concentration during early development, in agreement with the threshold model, but subsequently adapts partially in response to altered bicoid dosage, driving segmentation patterns towards their wild-type positions. This dynamic response requires other maternal regulators such as Torso and Nanos, suggesting that integration of maternal input information is not achieved through molecular interactions at the time of readout, but through the subsequent collective interplay of the network.

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